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: 9.34). 03/2008; 20(2):452-70. DOI: 10.1105/tpc.107.054718
Source: PubMed


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, Oct 07, 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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    • "A recent improvement for fluorescence staining to detect PP TCs in Arabidopsis leaves has been the use of Aniline Blue rather than Calcofluor White. Callose is an abundant component of the electron translucent outer layer of wall ingrowths in both epidermal TCs of V. faba cotyledons (Vaughn et al., 2007) and Arabidopsis PP TCs (Maeda et al., 2006, 2008). Other than being deposited in sieve plates, callose is mostly absent from other tissues in unwounded leaves, thus giving superior signal-to-noise staining of PP TCs compared to Calcofluor White (Figures 1E, F). "
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    ABSTRACT: In species performing apoplasmic loading, phloem cells adjacent to sieve elements often develop into transfer cells (TCs) with wall ingrowths. The highly invaginated wall ingrowths serve to amplify plasma membrane surface area to achieve increased rates of apoplasmic transport, and may also serve as physical barriers to deter pathogen invasion. Wall ingrowth formation in TCs therefore plays an important role in phloem biology, however, the transcriptional switches regulating the deposition of this unique example of highly localized wall building remain unknown. Phloem parenchyma (PP) TCs in Arabidopsis veins provide an experimental system to identify such switches. The extent of ingrowth deposition responds to various abiotic and applied stresses, enabling bioinformatics to identify candidate regulatory genes. Furthermore, simple fluorescence staining of PP TCs in leaves enables phenotypic analysis of relevant mutants. Combining these approaches resulted in the identification of GIGANTEA as a regulatory component in the pathway controlling wall ingrowth development in PP TCs. Further utilization of this approach has identified two NAC (NAM, ATAF1/2 and CUC2)-domain and two MYB-related genes as putative transcriptional switches regulating wall ingrowth deposition in these cells.
    Frontiers in Plant Science 04/2013; 4:102. DOI:10.3389/fpls.2013.00102 · 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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