Arabidopsis sfd Mutants Affect Plastidic Lipid Composition and Suppress Dwarfing, Cell Death, and the Enhanced Disease Resistance Phenotypes Resulting from the Deficiency of a Fatty Acid Desaturase

Nandi, Ashis Kumar; Krothapalli, Kartikeya; Buseman, Christen M.; Li, Maoyin; Welti, Ruth; Enyedi, Alexander J.; Shah, Jyoti

doi:10.1105/tpc.015529

Cited by 93 publications

(92 citation statements)

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“…Our earlier work has shown that a mutation in the SSI2-encoded S-ACP-DES affects many cellular responses in the plant, and we have demonstrated that the altered defense-related phenotypes in ssi2 plants are specifically associated with their low 18:1 levels (12,(15)(16)(17)22). Previous research by Nandi et al (37,38) has implicated a reduction in hexadecatrienoic acid (16:3) to be responsible for restoration of ssi2 phenotypes. However, several results contradict a role for 16:3.…”

Section: Discussionmentioning

confidence: 99%

Plastidial fatty acid levels regulate resistance gene-dependent defense signaling in Arabidopsis

Chandra-Shekara

Venugopal

Barman

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

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In Arabidopsis, resistance to Turnip Crinkle Virus (TCV) depends on the resistance (R) gene, HRT, and the recessive locus rrt. Resistance also depends on salicylic acid (SA), EDS1, and PAD4. Exogenous application of SA confers resistance in RRT-containing plants by increasing HRT transcript levels in a PAD4-dependent manner. Here we report that reduction of oleic acid (18:1) can also induce HRT gene expression and confer resistance to TCV. However, the 18:1-regulated pathway is independent of SA, rrt, EDS1, and PAD4. Reducing the levels of 18:1, via a mutation in the SSI2-encoded stearoyl-acyl carrier protein-desaturase, or by exogenous application of glycerol, increased transcript levels of HRT as well as several other R genes. Second-site mutations in the ACT1-encoded glycerol-3-phosphate acyltransferase or GLY1-encoded glycerol-3-phosphate dehydrogenase restored 18:1 levels in HRT ssi2 plants and reestablished a dependence on rrt. Resistance to TCV and HRT gene expression in HRT act1 plants was inducible by SA but not by glycerol, whereas that in HRT pad4 plants was inducible by glycerol but not by SA. The low 18:1-mediated induction of R gene expression was also dependent on ACT1 but independent of EDS1, PAD4, and RAR1. Intriguingly, TCV inoculation did not activate this 18:1-regulated pathway in HRT plants, but instead resulted in the induction of several genes that encode 18:1-synthesizing isozymes. These results suggest that the 18:1-regulated pathway may be specifically targeted during pathogen infection and that altering 18:1 levels may serve as a unique strategy for promoting disease resistance.glycerol ͉ salicylic acid ͉ stearoyl-acyl carrier protein-desaturase ͉ Turnip Crinkle Virus ͉ ssi2 P lants respond to pathogen perception by triggering a cascade of responses. Perception involves strain-specific detection of a pathogen-encoded elicitor, through direct or indirect interaction, with the corresponding resistance (R) gene product. Such an interaction (also known as incompatible interaction) triggers one or more defense signaling pathways and is often associated with the induction of the hypersensitive response (HR) at the site of pathogen entry. HR is one of the first visible manifestations of the host-induced defense response and is thought to prevent development and movement of the pathogen by inducing deliberate death of the infected cells. R protein-mediated recognition of pathogen can also lead to the accumulation of various phytohormones including salicylic acid (SA), jasmonic acid, and/or ethylene, which in turn signal the activation of defense gene expression. Each hormone activates a specific pathway, and these act individually, synergistically, or antagonistically, depending on the pathogen involved, the ultimate effect of which confers disease resistance and prevents spread of the pathogen to uninoculated parts of the plant.Several components of the SA-mediated pathway have been identified, mutations in which lead to enhanced susceptibility to various pathogens [supporting information (SI...

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Section: Discussionmentioning

confidence: 99%

Plastidial fatty acid levels regulate resistance gene-dependent defense signaling in Arabidopsis

Chandra-Shekara

Venugopal

Barman

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

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“…The down-regulation of the expression of genes encoding stearoyl-ACP desaturases has been repeatedly reported and is associated with changes in fatty acid composition and alterations in various physiological traits and growth of mutants or transgenic plants (Knutzon et al 1992;Lightner et al 1994a, b;Merlo et al 1998;Kachroo et al 2001;Nandi et al 2003). However, there are relatively few data concerning up-regulation of the same genes.…”

Section: Discussionmentioning

confidence: 99%

Transplastomic tobacco plants expressing a fatty acid desaturase gene exhibit altered fatty acid profiles and improved cold tolerance

Craig¹,

Lenzi²,

Scotti³

et al. 2008

Transgenic Res

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The possibility of altering the unsaturation level of fatty acids in plant lipids by genetic transformation has implications for the stress tolerance of higher plants as well as for their nutritional value and industrial utilisation. While the integration and expression of transgenes in the plastome has several potential advantages over nuclear transformation, very few attempts have been made to manipulate fatty acid biosynthesis using plastid transformation. We produced transplastomic tobacco plants that express a D 9 desaturase gene from either the wild potato species Solanum commersonii or the cyanobacterium Anacystis nidulans, using PEG-mediated DNA uptake by protoplasts. Incorporation of chloroplast antibioticinsensitive point mutations in the transforming DNA was used to select transformants. The presence of the transcript and the D 9 desaturase protein in transplastomic plants was confirmed by northern and western blot analyses. In comparison with control plants, transplastomic plants showed altered fatty acid profiles and an increase in their unsaturation level both in leaves and seeds. The two transgenes produced comparable results. The results obtained demonstrate the feasibility of using plastid transformation to engineer lipid metabolic pathways in both vegetative and reproductive tissues and suggest an increase of cold tolerance in transplastomic plants showing altered leaf fatty acid profiles. This is the first example of transplastomic plants expressing an agronomically relevant gene produced with the ''binding-type'' vectors, which do not contain a heterologous marker gene. In fact, the transplastomic plants expressing the S. commersonii gene contain only plant-derived sequences, a clear attraction from a public acceptability perspective.

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“…Alternatively, slower growth of the mutant may be the result of reduced synthesis of other critical components such as sphingolipids, cutin, and waxes, or lower rates of acylation reactions. In addition, lipid-derived signaling molecules that affect growth could be affected in the mutant (Nandi et al, 2003). When fatb-ko plants were grown at a range of different temperatures, no suppression of the fatb-ko growth phenotype was observed, suggesting that changes in the bulk properties of cellular membranes were not the main factor affecting plant performance (Bonaventure et al, 2003).…”

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confidence: 99%

Metabolic Responses to the Reduction in Palmitate Caused by Disruption of the FATB Gene in Arabidopsis

et al. 2004

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Disruption of the FATB gene in Arabidopsis results in a two-thirds reduction in saturated fatty acids, largely palmitate, in the leaf extra-plastidic phospholipids and a reduction in the growth rate of the mutant compared to wild type (Bonaventure G, Salas JJ, Pollard MR, Ohlrogge JB [2003] Plant Cell 15: 1020-1033. In this study, we report that although fatb-ko seedlings grow more slowly than wild type, the rate of fatty acid synthesis in leaves of the mutant increases by 40%. This results in approximately the same amount of palmitate exported from the plastid as in wild type but an increase in oleate export of about 55%. To maintain constant amounts of fatty acids in leaves, thereby counterbalancing their higher rate of production, the mutant also increases its rate of fatty acid degradation. Although fatb-ko leaves have higher rates of fatty acid synthesis and turnover, the relative proportions of membrane lipids are similar to wild type. Thus, homeostatic mechanisms to preserve membrane compositions compensate for substantial changes in rates of fatty acid and glycerolipid metabolism in the mutant. Pulse-chase labeling studies show that in fatb-ko leaves there is a net increase in the synthesis of both prokaryotic and eukaryotic lipids and consequently of their turnover. The net loss of palmitate from phosphatidylcholine plus phosphatidylethanolamine is similar for wild type and mutant, suggesting that mechanisms are not present that can preferentially preserve the saturated fatty acids. In summary, the leaf cell responds to the loss of saturated fatty acid production in the fatb-ko mutant by increasing both fatty acid synthesis and degradation, but in doing so the mechanisms for increased fatty acid turnover contribute to the lowering of the percentage of saturated fatty acids found in eukaryotic lipids.In plants, the major site for de novo fatty acid synthesis (FAS) occurs in the plastid (Ohlrogge et al., 1979). Fatty acids are either utilized in this organelle or exported to supply diverse cytoplasmic biosynthetic pathways and cellular processes. Production of fatty acids for export depends on the activity of acyl-ACP thioesterases (FATs) that hydrolyze acyl-acyl carrier protein (acyl-ACP) to release free fatty acids and ACP (for review, see Voelker et al., 1997). After export, the free fatty acids are re-esterified to CoA to form the cytosolic acyl-CoA pool (Pollard and Ohlrogge, 1999). In mesophyll cells, acyl-CoAs are primarily used for the biosynthesis of membrane glycerolipids in the endoplasmic reticulum (Browse and Somerville, 1991). However, in other cell types exported fatty acids have different fates. For example, in embryo cells of oilseeds, the major fraction is incorporated into triacylglycerols, while in epidermal cells a large fraction is utilized for the synthesis of waxes and cutin (Post-Beittenmiller, 1996;Kolattukudy, 2003). Furthermore, all cells synthesize sphingolipids (Lynch, 1993), and we recently estimated that as much as 30% to 40% of exported palmitate is needed for sphingoid ba...

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Arabidopsis sfd Mutants Affect Plastidic Lipid Composition and Suppress Dwarfing, Cell Death, and the Enhanced Disease Resistance Phenotypes Resulting from the Deficiency of a Fatty Acid Desaturase

Cited by 93 publications

References 65 publications

Plastidial fatty acid levels regulate resistance gene-dependent defense signaling in Arabidopsis

Plastidial fatty acid levels regulate resistance gene-dependent defense signaling in Arabidopsis

Transplastomic tobacco plants expressing a fatty acid desaturase gene exhibit altered fatty acid profiles and improved cold tolerance

Metabolic Responses to the Reduction in Palmitate Caused by Disruption of the FATB Gene in Arabidopsis

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