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Salicylic acid modulates levels of phosphoinositide dependent-phospholipase C substrates and products to remodel the Arabidopsis suspension cell transcriptome.

Ruelland E, Pokotylo I, Djafi N, Cantrel C, Repellin A, Zachowski A - Front Plant Sci (2014)

Bottom Line: We confirm here that in Arabidopsis suspension cells SA treatment leads to an increase in phosphoinositides, then demonstrate that SA leads to a significant 20% decrease in phosphatidic acid, indicative of a decrease in PI-PLC products.Alterations in the levels of a second set of genes, mostly SA-repressed genes, could be related to decreases in PI-PLC products that occur in response to SA action.We propose a model in which SA inhibits PI-PLC activity and alters levels of PI-PLC products and substrates, thereby regulating gene expression divergently.

View Article: PubMed Central - PubMed

Affiliation: Université Paris-Est Créteil, Institut d'Ecologie et des Sciences de l'Environnement de Paris Créteil, France ; Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7618, Institut d'Ecologie et des Sciences de l'Environnement de Paris Créteil, France.

ABSTRACT
Basal phosphoinositide-dependent phospholipase C (PI-PLC) activity controls gene expression in Arabidopsis suspension cells and seedlings. PI-PLC catalyzes the production of phosphorylated inositol and diacylglycerol (DAG) from phosphoinositides. It is not known how PI-PLC regulates the transcriptome although the action of DAG-kinase (DGK) on DAG immediately downstream from PI-PLC is responsible for some of the regulation. We previously established a list of genes whose expression is affected in the presence of PI-PLC inhibitors. Here this list of genes was used as a signature in similarity searches of curated plant hormone response transcriptome data. The strongest correlations obtained with the inhibited PI-PLC signature were with salicylic acid (SA) treatments. We confirm here that in Arabidopsis suspension cells SA treatment leads to an increase in phosphoinositides, then demonstrate that SA leads to a significant 20% decrease in phosphatidic acid, indicative of a decrease in PI-PLC products. Previous sets of microarray data were re-assessed. The SA response of one set of genes was dependent on phosphoinositides. Alterations in the levels of a second set of genes, mostly SA-repressed genes, could be related to decreases in PI-PLC products that occur in response to SA action. Together, the two groups of genes comprise at least 40% of all SA-responsive genes. Overall these two groups of genes are distinct in the functional categories of the proteins they encode, their promoter cis-elements and their regulation by DGK or phospholipase D. SA-regulated genes dependent on phosphoinositides are typical SA response genes while those with an SA response that is possibly dependent on PI-PLC products are less SA-specific. We propose a model in which SA inhibits PI-PLC activity and alters levels of PI-PLC products and substrates, thereby regulating gene expression divergently.

No MeSH data available.


Categorization of all SA-induced genes, cluster A genes and cluster B genes according to the molecular functions (A), Biological processes (B) and Cellular components (C) they are associated with. The data are normalized to category frequencies in the Arabidopsis genome dataset. The mean and SD for 100 bootstraps of the input were calculated. For cellular component analysis, two scales are used for clarity.
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Figure 8: Categorization of all SA-induced genes, cluster A genes and cluster B genes according to the molecular functions (A), Biological processes (B) and Cellular components (C) they are associated with. The data are normalized to category frequencies in the Arabidopsis genome dataset. The mean and SD for 100 bootstraps of the input were calculated. For cellular component analysis, two scales are used for clarity.

Mentions: The stringent clusters of genes are selected subsets of genes induced or repressed by SA. Some of the gene names from the four clusters are listed in Figure 7 with more precise details of their individual expression profiles. The genes of the different stringent clusters were classified according to gene ontology (GO) classes of “Biological processes,” “Molecular function,” and “Cellular component.” The results were normalized to the frequency of each class over the entire genome (Figure 8).


Salicylic acid modulates levels of phosphoinositide dependent-phospholipase C substrates and products to remodel the Arabidopsis suspension cell transcriptome.

Ruelland E, Pokotylo I, Djafi N, Cantrel C, Repellin A, Zachowski A - Front Plant Sci (2014)

Categorization of all SA-induced genes, cluster A genes and cluster B genes according to the molecular functions (A), Biological processes (B) and Cellular components (C) they are associated with. The data are normalized to category frequencies in the Arabidopsis genome dataset. The mean and SD for 100 bootstraps of the input were calculated. For cellular component analysis, two scales are used for clarity.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4227474&req=5

Figure 8: Categorization of all SA-induced genes, cluster A genes and cluster B genes according to the molecular functions (A), Biological processes (B) and Cellular components (C) they are associated with. The data are normalized to category frequencies in the Arabidopsis genome dataset. The mean and SD for 100 bootstraps of the input were calculated. For cellular component analysis, two scales are used for clarity.
Mentions: The stringent clusters of genes are selected subsets of genes induced or repressed by SA. Some of the gene names from the four clusters are listed in Figure 7 with more precise details of their individual expression profiles. The genes of the different stringent clusters were classified according to gene ontology (GO) classes of “Biological processes,” “Molecular function,” and “Cellular component.” The results were normalized to the frequency of each class over the entire genome (Figure 8).

Bottom Line: We confirm here that in Arabidopsis suspension cells SA treatment leads to an increase in phosphoinositides, then demonstrate that SA leads to a significant 20% decrease in phosphatidic acid, indicative of a decrease in PI-PLC products.Alterations in the levels of a second set of genes, mostly SA-repressed genes, could be related to decreases in PI-PLC products that occur in response to SA action.We propose a model in which SA inhibits PI-PLC activity and alters levels of PI-PLC products and substrates, thereby regulating gene expression divergently.

View Article: PubMed Central - PubMed

Affiliation: Université Paris-Est Créteil, Institut d'Ecologie et des Sciences de l'Environnement de Paris Créteil, France ; Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7618, Institut d'Ecologie et des Sciences de l'Environnement de Paris Créteil, France.

ABSTRACT
Basal phosphoinositide-dependent phospholipase C (PI-PLC) activity controls gene expression in Arabidopsis suspension cells and seedlings. PI-PLC catalyzes the production of phosphorylated inositol and diacylglycerol (DAG) from phosphoinositides. It is not known how PI-PLC regulates the transcriptome although the action of DAG-kinase (DGK) on DAG immediately downstream from PI-PLC is responsible for some of the regulation. We previously established a list of genes whose expression is affected in the presence of PI-PLC inhibitors. Here this list of genes was used as a signature in similarity searches of curated plant hormone response transcriptome data. The strongest correlations obtained with the inhibited PI-PLC signature were with salicylic acid (SA) treatments. We confirm here that in Arabidopsis suspension cells SA treatment leads to an increase in phosphoinositides, then demonstrate that SA leads to a significant 20% decrease in phosphatidic acid, indicative of a decrease in PI-PLC products. Previous sets of microarray data were re-assessed. The SA response of one set of genes was dependent on phosphoinositides. Alterations in the levels of a second set of genes, mostly SA-repressed genes, could be related to decreases in PI-PLC products that occur in response to SA action. Together, the two groups of genes comprise at least 40% of all SA-responsive genes. Overall these two groups of genes are distinct in the functional categories of the proteins they encode, their promoter cis-elements and their regulation by DGK or phospholipase D. SA-regulated genes dependent on phosphoinositides are typical SA response genes while those with an SA response that is possibly dependent on PI-PLC products are less SA-specific. We propose a model in which SA inhibits PI-PLC activity and alters levels of PI-PLC products and substrates, thereby regulating gene expression divergently.

No MeSH data available.