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Boolean modeling of transcriptome data reveals novel modes of heterotrimeric G-protein action.

Pandey S, Wang RS, Wilson L, Li S, Zhao Z, Gookin TE, Assmann SM, Albert R - Mol. Syst. Biol. (2010)

Bottom Line: Although G-protein control of the transcriptome has received little attention to date in any system, transcriptome analysis allows us to search for potentially uncommon yet significant signaling mechanisms.We find that (1) classical mechanisms of G-protein signaling are well represented.Our method holds significant promise for analyzing analogous 'switch-like' signal transduction events in any organism.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Pennsylvania State University, University Park, PA 16802, USA.

ABSTRACT
Heterotrimeric G-proteins mediate crucial and diverse signaling pathways in eukaryotes. Here, we generate and analyze microarray data from guard cells and leaves of G-protein subunit mutants of the model plant Arabidopsis thaliana, with or without treatment with the stress hormone, abscisic acid. Although G-protein control of the transcriptome has received little attention to date in any system, transcriptome analysis allows us to search for potentially uncommon yet significant signaling mechanisms. We describe the theoretical Boolean mechanisms of G-protein x hormone regulation, and then apply a pattern matching approach to associate gene expression profiles with Boolean models. We find that (1) classical mechanisms of G-protein signaling are well represented. Conversely, some theoretical regulatory modes of the G-protein are not supported; (2) a new mechanism of G-protein signaling is revealed, in which Gbeta regulates gene expression identically in the presence or absence of Galpha; (3) guard cells and leaves favor different G-protein modes in transcriptome regulation, supporting system specificity of G-protein signaling. Our method holds significant promise for analyzing analogous 'switch-like' signal transduction events in any organism.

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Gene expression pattern for a classical I G-protein regulatory mode coupling with ABA in leaves. The 20 genes with the highest correlation scores (out of 86) are shown. TAIR (http://www.arabidopsis.org/) derived accession numbers and a brief description of the genes are shown next to the heat map.
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f6: Gene expression pattern for a classical I G-protein regulatory mode coupling with ABA in leaves. The 20 genes with the highest correlation scores (out of 86) are shown. TAIR (http://www.arabidopsis.org/) derived accession numbers and a brief description of the genes are shown next to the heat map.

Mentions: In leaves, A2 (and/or A15)-related regulatory modes are the most prevalent: B2(ABA, A2)=ABA and (GPA1 and AGB1)=ABA and A2, B15(ABA, A2)=not ABA or not A2, B5(ABA, A2)=not ABA and A2, and B12(ABA, A2)=ABA or not A2. These regulatory modes are consistent with Figure 1D where the mediator M1 is synergistically regulated by GPA1 and AGB1 (classical I G-protein regulatory mechanisms) and the second mediator M2 is combinatorially regulated by M1 and ABA. Figure 6 illustrates one of these well-supported modes, B2(ABA, A2)=ABA and (GPA1 and AGB1), in which gene expression is highest in wild type plus ABA, due to a requirement for both a wild-type G-protein complement and ABA treatment to elevate transcript levels. There are only three genes in the G-protein-only category in leaves, and two of them are the G-protein subunits GPA1 and AGB1 included by default; the third is At3G12730, a MYB family transcription factor. This suggests that in leaves there are very few genes that are regulated by the G-protein independently of ABA signaling and instead the co-regulatory mode of the G-protein and ABA is prevalent.


Boolean modeling of transcriptome data reveals novel modes of heterotrimeric G-protein action.

Pandey S, Wang RS, Wilson L, Li S, Zhao Z, Gookin TE, Assmann SM, Albert R - Mol. Syst. Biol. (2010)

Gene expression pattern for a classical I G-protein regulatory mode coupling with ABA in leaves. The 20 genes with the highest correlation scores (out of 86) are shown. TAIR (http://www.arabidopsis.org/) derived accession numbers and a brief description of the genes are shown next to the heat map.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2913393&req=5

f6: Gene expression pattern for a classical I G-protein regulatory mode coupling with ABA in leaves. The 20 genes with the highest correlation scores (out of 86) are shown. TAIR (http://www.arabidopsis.org/) derived accession numbers and a brief description of the genes are shown next to the heat map.
Mentions: In leaves, A2 (and/or A15)-related regulatory modes are the most prevalent: B2(ABA, A2)=ABA and (GPA1 and AGB1)=ABA and A2, B15(ABA, A2)=not ABA or not A2, B5(ABA, A2)=not ABA and A2, and B12(ABA, A2)=ABA or not A2. These regulatory modes are consistent with Figure 1D where the mediator M1 is synergistically regulated by GPA1 and AGB1 (classical I G-protein regulatory mechanisms) and the second mediator M2 is combinatorially regulated by M1 and ABA. Figure 6 illustrates one of these well-supported modes, B2(ABA, A2)=ABA and (GPA1 and AGB1), in which gene expression is highest in wild type plus ABA, due to a requirement for both a wild-type G-protein complement and ABA treatment to elevate transcript levels. There are only three genes in the G-protein-only category in leaves, and two of them are the G-protein subunits GPA1 and AGB1 included by default; the third is At3G12730, a MYB family transcription factor. This suggests that in leaves there are very few genes that are regulated by the G-protein independently of ABA signaling and instead the co-regulatory mode of the G-protein and ABA is prevalent.

Bottom Line: Although G-protein control of the transcriptome has received little attention to date in any system, transcriptome analysis allows us to search for potentially uncommon yet significant signaling mechanisms.We find that (1) classical mechanisms of G-protein signaling are well represented.Our method holds significant promise for analyzing analogous 'switch-like' signal transduction events in any organism.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Pennsylvania State University, University Park, PA 16802, USA.

ABSTRACT
Heterotrimeric G-proteins mediate crucial and diverse signaling pathways in eukaryotes. Here, we generate and analyze microarray data from guard cells and leaves of G-protein subunit mutants of the model plant Arabidopsis thaliana, with or without treatment with the stress hormone, abscisic acid. Although G-protein control of the transcriptome has received little attention to date in any system, transcriptome analysis allows us to search for potentially uncommon yet significant signaling mechanisms. We describe the theoretical Boolean mechanisms of G-protein x hormone regulation, and then apply a pattern matching approach to associate gene expression profiles with Boolean models. We find that (1) classical mechanisms of G-protein signaling are well represented. Conversely, some theoretical regulatory modes of the G-protein are not supported; (2) a new mechanism of G-protein signaling is revealed, in which Gbeta regulates gene expression identically in the presence or absence of Galpha; (3) guard cells and leaves favor different G-protein modes in transcriptome regulation, supporting system specificity of G-protein signaling. Our method holds significant promise for analyzing analogous 'switch-like' signal transduction events in any organism.

Show MeSH
Related in: MedlinePlus