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An integrated genetic, genomic and systems approach defines gene networks regulated by the interaction of light and carbon signaling pathways in Arabidopsis.

Thum KE, Shin MJ, GutiƩrrez RA, Mukherjee I, Katari MS, Nero D, Shasha D, Coruzzi GM - BMC Syst Biol (2008)

Bottom Line: One transcription factor, HAT22 appears to be a regulatory "hub" in the cli186 network as it shows regulatory connections linking a metabolic network of genes involved in "amino acid metabolism", "C-compound/carbohydrate metabolism" and "glycolysis/gluconeogenesis".The global misregulation of gene networks controlled by light and carbon signaling in cli186 indicates that it represents one of the first Arabidopsis mutants isolated that is specifically disrupted in the integration of both carbon and light signals to control the regulation of metabolic, developmental and regulatory genes.The network analysis of misregulated genes suggests that CLI186 acts to integrate light and carbon signaling interactions and is a master regulator connecting the regulation of a host of downstream metabolic and regulatory processes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biology, New York University, New York, NY, 10003, USA. karen.thum@gmail.com

ABSTRACT

Background: Light and carbon are two important interacting signals affecting plant growth and development. The mechanism(s) and/or genes involved in sensing and/or mediating the signaling pathways involving these interactions are unknown. This study integrates genetic, genomic and systems approaches to identify a genetically perturbed gene network that is regulated by the interaction of carbon and light signaling in Arabidopsis.

Results: Carbon and light insensitive (cli) mutants were isolated. Microarray data from cli186 is analyzed to identify the genes, biological processes and gene networks affected by the integration of light and carbon pathways. Analysis of this data reveals 966 genes regulated by light and/or carbon signaling in wild-type. In cli186, 216 of these light/carbon regulated genes are misregulated in response to light and/or carbon treatments where 78% are misregulated in response to light and carbon interactions. Analysis of the gene lists show that genes in the biological processes "energy" and "metabolism" are over-represented among the 966 genes regulated by carbon and/or light in wild-type, and the 216 misregulated genes in cli186. To understand connections among carbon and/or light regulated genes in wild-type and the misregulated genes in cli186, the microarray data is interpreted in the context of metabolic and regulatory networks. The network created from the 966 light/carbon regulated genes in wild-type, reveals that cli186 is affected in the light and/or carbon regulation of a network of 60 connected genes, including six transcription factors. One transcription factor, HAT22 appears to be a regulatory "hub" in the cli186 network as it shows regulatory connections linking a metabolic network of genes involved in "amino acid metabolism", "C-compound/carbohydrate metabolism" and "glycolysis/gluconeogenesis".

Conclusion: The global misregulation of gene networks controlled by light and carbon signaling in cli186 indicates that it represents one of the first Arabidopsis mutants isolated that is specifically disrupted in the integration of both carbon and light signals to control the regulation of metabolic, developmental and regulatory genes. The network analysis of misregulated genes suggests that CLI186 acts to integrate light and carbon signaling interactions and is a master regulator connecting the regulation of a host of downstream metabolic and regulatory processes.

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A metabolic and regulatory sub-network created from the 216 misregulated genes in cli186. This is a sub-network of the 216 misregulated genes that was extracted from the larger multinetwork created using the 966 L/C regulated genes in WT [see Additional file 5] and visualized using Cytoscape [54]. Nodes representing genes (blue hexagons), genes annotated to be transcription factors (green diamonds) or metabolites (peach circles) are connected via edges. The type of edge indicates if the interaction is metabolic (grey arrows), protein-DNA regulation (red arrows) or protein-protein (blue dashed lines). Protein-DNA interactions are supported by the presence of one or more binding sites within the promoter of that gene for that particular transcription factor (see Methods). This is a connected network comprised of 60/216 misregulated genes in cli186 in which all of the nodes represented are misregulated in cli186.
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Figure 3: A metabolic and regulatory sub-network created from the 216 misregulated genes in cli186. This is a sub-network of the 216 misregulated genes that was extracted from the larger multinetwork created using the 966 L/C regulated genes in WT [see Additional file 5] and visualized using Cytoscape [54]. Nodes representing genes (blue hexagons), genes annotated to be transcription factors (green diamonds) or metabolites (peach circles) are connected via edges. The type of edge indicates if the interaction is metabolic (grey arrows), protein-DNA regulation (red arrows) or protein-protein (blue dashed lines). Protein-DNA interactions are supported by the presence of one or more binding sites within the promoter of that gene for that particular transcription factor (see Methods). This is a connected network comprised of 60/216 misregulated genes in cli186 in which all of the nodes represented are misregulated in cli186.

Mentions: To gain a gene-by-gene network view of the connectivity of the 216 L/C misregulated genes in cli186, the 216 genes were used to directly query the Arabidopsis multinetwork (Figure 3) [see Additional file 7]. A number of interactions are visualized within this sub-network including: (1) metabolic networks (2) protein:protein interaction networks and (3) protein:DNA regulatory interaction networks [21] (see Methods). Nodes representing genes (blue hexagons), genes annotated to be transcription factors (green diamonds) or metabolites (peach circles) are connected via edges. The type of edge indicates if the interaction is metabolic (black arrows), protein:DNA regulation (red arrows) or protein-protein interactions (blue dashed lines). Predicted transcription factor target gene edge connections are based on interactions available from AGRIS [39], the interolog and regulogs described previously [40] and the statistical over-representation of the transcription factor binding sites within the target gene promoter and the correlation (p < 0.01 and r > 0.5) of expression of the transcription factor and target gene across all 16 experiments (see Methods). This analysis shows one large network comprised of 60/216 genes, all of which are L/C misregulated in cli186.


An integrated genetic, genomic and systems approach defines gene networks regulated by the interaction of light and carbon signaling pathways in Arabidopsis.

Thum KE, Shin MJ, GutiƩrrez RA, Mukherjee I, Katari MS, Nero D, Shasha D, Coruzzi GM - BMC Syst Biol (2008)

A metabolic and regulatory sub-network created from the 216 misregulated genes in cli186. This is a sub-network of the 216 misregulated genes that was extracted from the larger multinetwork created using the 966 L/C regulated genes in WT [see Additional file 5] and visualized using Cytoscape [54]. Nodes representing genes (blue hexagons), genes annotated to be transcription factors (green diamonds) or metabolites (peach circles) are connected via edges. The type of edge indicates if the interaction is metabolic (grey arrows), protein-DNA regulation (red arrows) or protein-protein (blue dashed lines). Protein-DNA interactions are supported by the presence of one or more binding sites within the promoter of that gene for that particular transcription factor (see Methods). This is a connected network comprised of 60/216 misregulated genes in cli186 in which all of the nodes represented are misregulated in cli186.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2335094&req=5

Figure 3: A metabolic and regulatory sub-network created from the 216 misregulated genes in cli186. This is a sub-network of the 216 misregulated genes that was extracted from the larger multinetwork created using the 966 L/C regulated genes in WT [see Additional file 5] and visualized using Cytoscape [54]. Nodes representing genes (blue hexagons), genes annotated to be transcription factors (green diamonds) or metabolites (peach circles) are connected via edges. The type of edge indicates if the interaction is metabolic (grey arrows), protein-DNA regulation (red arrows) or protein-protein (blue dashed lines). Protein-DNA interactions are supported by the presence of one or more binding sites within the promoter of that gene for that particular transcription factor (see Methods). This is a connected network comprised of 60/216 misregulated genes in cli186 in which all of the nodes represented are misregulated in cli186.
Mentions: To gain a gene-by-gene network view of the connectivity of the 216 L/C misregulated genes in cli186, the 216 genes were used to directly query the Arabidopsis multinetwork (Figure 3) [see Additional file 7]. A number of interactions are visualized within this sub-network including: (1) metabolic networks (2) protein:protein interaction networks and (3) protein:DNA regulatory interaction networks [21] (see Methods). Nodes representing genes (blue hexagons), genes annotated to be transcription factors (green diamonds) or metabolites (peach circles) are connected via edges. The type of edge indicates if the interaction is metabolic (black arrows), protein:DNA regulation (red arrows) or protein-protein interactions (blue dashed lines). Predicted transcription factor target gene edge connections are based on interactions available from AGRIS [39], the interolog and regulogs described previously [40] and the statistical over-representation of the transcription factor binding sites within the target gene promoter and the correlation (p < 0.01 and r > 0.5) of expression of the transcription factor and target gene across all 16 experiments (see Methods). This analysis shows one large network comprised of 60/216 genes, all of which are L/C misregulated in cli186.

Bottom Line: One transcription factor, HAT22 appears to be a regulatory "hub" in the cli186 network as it shows regulatory connections linking a metabolic network of genes involved in "amino acid metabolism", "C-compound/carbohydrate metabolism" and "glycolysis/gluconeogenesis".The global misregulation of gene networks controlled by light and carbon signaling in cli186 indicates that it represents one of the first Arabidopsis mutants isolated that is specifically disrupted in the integration of both carbon and light signals to control the regulation of metabolic, developmental and regulatory genes.The network analysis of misregulated genes suggests that CLI186 acts to integrate light and carbon signaling interactions and is a master regulator connecting the regulation of a host of downstream metabolic and regulatory processes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biology, New York University, New York, NY, 10003, USA. karen.thum@gmail.com

ABSTRACT

Background: Light and carbon are two important interacting signals affecting plant growth and development. The mechanism(s) and/or genes involved in sensing and/or mediating the signaling pathways involving these interactions are unknown. This study integrates genetic, genomic and systems approaches to identify a genetically perturbed gene network that is regulated by the interaction of carbon and light signaling in Arabidopsis.

Results: Carbon and light insensitive (cli) mutants were isolated. Microarray data from cli186 is analyzed to identify the genes, biological processes and gene networks affected by the integration of light and carbon pathways. Analysis of this data reveals 966 genes regulated by light and/or carbon signaling in wild-type. In cli186, 216 of these light/carbon regulated genes are misregulated in response to light and/or carbon treatments where 78% are misregulated in response to light and carbon interactions. Analysis of the gene lists show that genes in the biological processes "energy" and "metabolism" are over-represented among the 966 genes regulated by carbon and/or light in wild-type, and the 216 misregulated genes in cli186. To understand connections among carbon and/or light regulated genes in wild-type and the misregulated genes in cli186, the microarray data is interpreted in the context of metabolic and regulatory networks. The network created from the 966 light/carbon regulated genes in wild-type, reveals that cli186 is affected in the light and/or carbon regulation of a network of 60 connected genes, including six transcription factors. One transcription factor, HAT22 appears to be a regulatory "hub" in the cli186 network as it shows regulatory connections linking a metabolic network of genes involved in "amino acid metabolism", "C-compound/carbohydrate metabolism" and "glycolysis/gluconeogenesis".

Conclusion: The global misregulation of gene networks controlled by light and carbon signaling in cli186 indicates that it represents one of the first Arabidopsis mutants isolated that is specifically disrupted in the integration of both carbon and light signals to control the regulation of metabolic, developmental and regulatory genes. The network analysis of misregulated genes suggests that CLI186 acts to integrate light and carbon signaling interactions and is a master regulator connecting the regulation of a host of downstream metabolic and regulatory processes.

Show MeSH