Tocopherols modulate extraplastidic polyunsaturated fatty acid metabolism in Arabidopsis at low temperature

Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824, USA.
The Plant Cell (Impact Factor: 9.58). 03/2008; 20(2):452-70. DOI: 10.1105/tpc.107.054718
Source: PubMed

ABSTRACT Tocopherols (vitamin E) are synthesized in plastids and have long been assumed to have essential functions restricted to these organelles. We previously reported that the vitamin e-deficient2 (vte2) mutant of Arabidopsis thaliana is defective in transfer cell wall development and photoassimilate transport at low temperature (LT). Here, we demonstrate that LT-treated vte2 has a distinct composition of polyunsaturated fatty acids (PUFAs): lower levels of linolenic acid (18:3) and higher levels of linoleic acid (18:2) compared with the wild type. Enhanced 18:3 oxidation was not involved, as indicated by the limited differences in oxidized lipid species between LT-treated vte2 and the wild type and by a lack of impact on the LT-induced vte2 phenotype in a vte2 fad3 fad7 fad8 quadruple mutant deficient in 18:3. PUFA changes in LT-treated vte2 occur primarily in phospholipids due to reduced conversion of dienoic to trienoic fatty acids in the endoplasmic reticulum (ER) pathway. Introduction of the ER fatty acid desaturase mutation, fad2, and to a lesser extent the plastidic fad6 mutation into the vte2 background suppressed the LT-induced vte2 phenotypes, including abnormal transfer cell wall development. These results provide biochemical and genetic evidence that plastid-synthesized tocopherols modulate ER PUFA metabolism early in the LT adaptation response of Arabidopsis.

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Available from: Dean DellaPenna, Aug 14, 2015
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    • "Previous and current studies have demonstrated that tocopherols are required for normal development of TCW ingrowths in Arabidopsis leaves in response to LT (Figure 6; Maeda et al., 2006, 2008). Although the precise underlying mechanism remains elusive, suppressor mutant analyses (Maeda et al., 2008; Song et al., 2010) and our recent transorganellar complementation study (Mehrshahi et al., 2013) suggest that deficiency in plastidlocalized tocopherols directly impacts ER membrane lipid biogenesis . Although speculative at this point, these alterations in ER membrane lipid metabolism may in turn impact other endomembrane-related processes, such as the massive increase in vesicular trafficking required for deposition of cell wall material in transfer cells at LT (Talbot et al., 2002; McCurdy et al., 2008). "
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    ABSTRACT: Tocopherols (vitamin E) are lipid-soluble antioxidants produced by all plants and algae, and many cyanobacteria, yet their functions in these photosynthetic organisms are still not fully understood. We have previously reported that the vitamin E deficient 2 (vte2) mutant of Arabidopsis thaliana is sensitive to low temperature (LT) due to impaired transfer cell wall (TCW) development and photoassimilate export associated with massive callose deposition in transfer cells of the phloem. To further understand the roles of tocopherols in LT induced TCW development we compared the global transcript profiles of vte2 and wild-type leaves during LT treatment. Tocopherol deficiency had no significant impact on global gene expression in permissive conditions, but significantly affected expression of 77 genes after 48 h of LT treatment. In vte2 relative to wild type, genes associated with solute transport were repressed, while those involved in various pathogen responses and cell wall modifications, including two members of callose synthase gene family, GLUCAN SYNTHASE LIKE 4 (GSL4) and GSL11, were induced. However, introduction of gsl4 or gsl11 mutations individually into the vte2 background did not suppress callose deposition or the overall LT-induced phenotypes of vte2. Intriguingly, introduction of a mutation disrupting GSL5, the major GSL responsible for pathogen-induced callose deposition, into vte2 substantially reduced vascular callose deposition at LT, but again had no effect on the photoassimilate export phenotype of LT-treated vte2. These results suggest that GSL5 plays a major role in TCW callose deposition in LT-treated vte2 but that this GSL5-dependent callose deposition is not the primary cause of the impaired photoassimilate export phenotype.
    Frontiers in Plant Science 02/2014; 5:46. DOI:10.3389/fpls.2014.00046 · 3.95 Impact Factor
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    • "Besides, thorough study of the functions of trienoic fatty acid (TFA) synthesis and thermal response during temperature shift (Gopalakrishnan Nair et al., 2009), FAD8 was also found in other biological functions, such as participation in pathogen defense as a precursor (Vijayan et al., 1998), adding sensitivity to abiotic stresses (Zhang et al., 2005), mediating tocopherol metabolism (Maeda et al., 2008) and increasing tolerance to drought (Torres-Franklin et al., 2009). In addition, the characterization of FAD8 in O. sativa L. suggested that it is involved in maintaining trienoic fatty acids level and sustaining stress tolerance at chilling conditions (Wang et al., 2006). "
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    ABSTRACT: As compared to untreated wild type Arabidopsis (WT), fad7/fad8 deficient Arabidopsis plant (SH1) showed less root elongation inhibition with 750 nM indole-3-acetic acid (IAA) treatment. This finding leads us to investigate the relationship between omega-3 fatty acid desaturase (FAD7 and FAD8) and IAA. We expressed a hemagglutinin-tagged-Brassica napusFAD8 (BnFAD8) gene in WT and SH1. Recovery of root elongation inhibition was observed in transformants derived from SH1 harboring native sequence of BnFAD8 (R2), and suggested that IAA response was affected by expression of BnFAD8. As compared to unmodified host plants (WT and SH1), transformants derived from WT harboring BnFAD8 (OE) and R2 exhibited flat cauline leaves. OE and R2 could also tolerate 2,4-dichlorophenoxyacetic acid (2,4-D) up to 500 nM, while WT and SH1 could not. In addition, OE showed more resistance to 5-methyl-tryptophan (5-MTRP) in culture test than WT. Further study regarding transcription level of gene CYP79B2, which was known to participate in IAA (auxin) biosynthesis indicated significant up-regulation in OE and R2. Overall, our results revealed that BnFAD8 was involved in multiple biological functions in Arabidopsis, including leaf morphological development, auxin biosynthesis and 2,4-D resistance.
    AFRICAN JOURNAL OF BIOTECHNOLOGY 03/2012; 11:2616-2624. · 0.57 Impact Factor
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    • "undergo a water loss during collision-induced dissociation to produce 18:4-O and 18:3-O, respectively. The dehydration allows 18:3-2O and 18:2-2O to be detected by scans for 18:4-O and 18:3-O, respectively (Buseman et al., 2006; Maeda et al., 2008). Thus, scanning for precursors of 291.2 (Pre 291.2) detects precursors of 18:4-O and 18:3-2O, scanning for Pre 293.2 detects precursors of 18:3-O and 18:2-2O, and scanning for Pre 295.2 detects precursors of 18:2-O. "
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    ABSTRACT: Direct infusion electrospray ionization triple quadrupole precursor scanning for three oxidized fatty acyl anions revealed 86 mass spectral peaks representing polar membrane lipids in extracts from Arabidopsis (Arabidopsis thaliana) infected with Pseudomonas syringae pv tomato DC3000 expressing AvrRpt2 (PstAvr). Quadrupole time-of-flight and Fourier transform ion cyclotron resonance mass spectrometry provided evidence for the presence of membrane lipids containing one or more oxidized acyl chains. The membrane lipids included molecular species of phosphatidylcholine, phosphatidylethanolamine, phosphatidylglycerol, digalactosyldiacylglycerol, monogalactosyldiacylglycerol, and acylated monogalactosyldiacylglycerol. The oxidized chains were identified at the level of chemical formula and included C(18)H(27)O(3) (abbreviated 18:4-O, to indicate four double bond equivalents and one oxygen beyond the carbonyl group), C(18)H(29)O(3) (18:3-O), C(18)H(31)O(3) (18:2-O), C(18)H(29)O(4) (18:3-2O), C(18)H(31)O(4) (18:2-2O), and C(16)H(23)O(3) (16:4-O). Mass spectral signals from the polar oxidized lipid (ox-lipid) species were quantified in extracts of Arabidopsis leaves subjected to wounding, infection by PstAvr, infection by a virulent strain of P. syringae, and low temperature. Ox-lipids produced low amounts of mass spectral signal, 0.1% to 3.2% as much as obtained in typical direct infusion profiling of normal-chain membrane lipids of the same classes. Analysis of the oxidized membrane lipid species and normal-chain phosphatidic acids indicated that stress-induced ox-lipid composition differs from the basal ox-lipid composition. Additionally, different stresses result in the production of varied amounts, different timing, and different compositional patterns of stress-induced membrane lipids. These data form the basis for a working hypothesis that the stress-specific signatures of ox-lipids, like those of oxylipins, are indicative of their functions.
    Plant physiology 11/2011; 158(1):324-39. DOI:10.1104/pp.111.190280 · 7.39 Impact Factor
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