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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.


Identification of genes whose expression characteristics are consistent with the clusters defined in Figure 3. Cluster A and B genes are SA-induced genes (A) while clusters C and D genes are SA-repressed genes (B).
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Figure 4: Identification of genes whose expression characteristics are consistent with the clusters defined in Figure 3. Cluster A and B genes are SA-induced genes (A) while clusters C and D genes are SA-repressed genes (B).

Mentions: From the 463 SA-induced genes in ACSC, we first discounted the 141 genes that were unaffected by treatments with edelfosine or W30 (Figure 4A). SA induction of cluster A genes is inhibited by W30 and not by W1, so they must be among the subset that is down-regulated in the SAW30 (SAW, SA + wortmannin) condition compared to the SAW1 condition. The basal level of regulation by PI-PLC substrates is already in place in resting cells, with SA-dependent PI-PLC inhibition only enhancing it. This basal regulation must be of the same nature and cannot be opposite to regulation in the presence of SA. The genes must be expressed at a lower level in W30 than in W1, so we can eliminate the 6 genes that are more expressed in W30 than in W1. The subset of 12 genes that are repressed by edelfosine is excluded, as this would not be compatible with basal PI-PLC substrates having a positive role. The remaining 114 genes thus form cluster A (Figure 4A). Cluster B genes are induced by an alleviation of repression via PI-PLC products. These genes must be induced by edelfosine and by W30, as both molecules inhibit the basal PI-PLC pathway. The effect of W30 in the presence of SA is either neutral or additive, so the 2 genes that are repressed by SAW30 compared to SAW1 can be excluded. Therefore, 51 genes have the characteristics of cluster B genes.


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)

Identification of genes whose expression characteristics are consistent with the clusters defined in Figure 3. Cluster A and B genes are SA-induced genes (A) while clusters C and D genes are SA-repressed genes (B).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 4: Identification of genes whose expression characteristics are consistent with the clusters defined in Figure 3. Cluster A and B genes are SA-induced genes (A) while clusters C and D genes are SA-repressed genes (B).
Mentions: From the 463 SA-induced genes in ACSC, we first discounted the 141 genes that were unaffected by treatments with edelfosine or W30 (Figure 4A). SA induction of cluster A genes is inhibited by W30 and not by W1, so they must be among the subset that is down-regulated in the SAW30 (SAW, SA + wortmannin) condition compared to the SAW1 condition. The basal level of regulation by PI-PLC substrates is already in place in resting cells, with SA-dependent PI-PLC inhibition only enhancing it. This basal regulation must be of the same nature and cannot be opposite to regulation in the presence of SA. The genes must be expressed at a lower level in W30 than in W1, so we can eliminate the 6 genes that are more expressed in W30 than in W1. The subset of 12 genes that are repressed by edelfosine is excluded, as this would not be compatible with basal PI-PLC substrates having a positive role. The remaining 114 genes thus form cluster A (Figure 4A). Cluster B genes are induced by an alleviation of repression via PI-PLC products. These genes must be induced by edelfosine and by W30, as both molecules inhibit the basal PI-PLC pathway. The effect of W30 in the presence of SA is either neutral or additive, so the 2 genes that are repressed by SAW30 compared to SAW1 can be excluded. Therefore, 51 genes have the characteristics of cluster B genes.

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.