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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 supernode network summarizes the biological processes regulated in wild-type and misregulated in cli186 by L/C treatments. Supernodes are created by collapsing genes into a category according to both their metabolic pathways and the first two words of their gene annotation. This supernode network was created from the large multinetwork analysis that contains the 966 L/C regulated genes in wild-type [see Additional file 6]. Blue nodes represent biological processes that contain genes that are under wild-type L/C regulation in wild-type and cli186. Yellow nodes represent biological processes in which at least one gene shows L/C misregulation in cli186. The size of the node indicates the number of genes within that particular biological process. Nodes are connected by either metabolic (grey lines), DNA:protein (red lines = positive correlation; green lines = negative correlation) or protein:protein (blue lines) interactions.
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Figure 2: A supernode network summarizes the biological processes regulated in wild-type and misregulated in cli186 by L/C treatments. Supernodes are created by collapsing genes into a category according to both their metabolic pathways and the first two words of their gene annotation. This supernode network was created from the large multinetwork analysis that contains the 966 L/C regulated genes in wild-type [see Additional file 6]. Blue nodes represent biological processes that contain genes that are under wild-type L/C regulation in wild-type and cli186. Yellow nodes represent biological processes in which at least one gene shows L/C misregulation in cli186. The size of the node indicates the number of genes within that particular biological process. Nodes are connected by either metabolic (grey lines), DNA:protein (red lines = positive correlation; green lines = negative correlation) or protein:protein (blue lines) interactions.

Mentions: To gain an understanding of how the various processes regulated by L/C in wild-type seedlings are connected to each other, and to determine which of these processes are perturbed by the cli186 mutation, a supernode network was created (Figure 2). Supernodes are created by collapsing multiple genes from a multinetwork into a single node, according to their annotation. For example, all genes annotated to the glycolysis/gluconeogenesis pathways are summarized in the network with a single node labeled "glycolysis/gluconeogenesis". The size of the node is proportional to the number of genes annotated to the corresponding node label. Gene edges from the large multinetwork are transferred to the supernode, and are summarized in the final supernode network by a single edge type between supernodes. The connectivity of the nodes are supported by edges that may be metabolic (grey line), protein-DNA (red line = positive correlation; green line = negative correlation) or protein-protein (blue dashed line) interactions or combinations thereof. Hence, this supernode analysis provides a summary of the biological processes that are L/C regulated in wild-type and those that are perturbed by the cli186 mutation and the connections between these processes.


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 supernode network summarizes the biological processes regulated in wild-type and misregulated in cli186 by L/C treatments. Supernodes are created by collapsing genes into a category according to both their metabolic pathways and the first two words of their gene annotation. This supernode network was created from the large multinetwork analysis that contains the 966 L/C regulated genes in wild-type [see Additional file 6]. Blue nodes represent biological processes that contain genes that are under wild-type L/C regulation in wild-type and cli186. Yellow nodes represent biological processes in which at least one gene shows L/C misregulation in cli186. The size of the node indicates the number of genes within that particular biological process. Nodes are connected by either metabolic (grey lines), DNA:protein (red lines = positive correlation; green lines = negative correlation) or protein:protein (blue lines) interactions.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 2: A supernode network summarizes the biological processes regulated in wild-type and misregulated in cli186 by L/C treatments. Supernodes are created by collapsing genes into a category according to both their metabolic pathways and the first two words of their gene annotation. This supernode network was created from the large multinetwork analysis that contains the 966 L/C regulated genes in wild-type [see Additional file 6]. Blue nodes represent biological processes that contain genes that are under wild-type L/C regulation in wild-type and cli186. Yellow nodes represent biological processes in which at least one gene shows L/C misregulation in cli186. The size of the node indicates the number of genes within that particular biological process. Nodes are connected by either metabolic (grey lines), DNA:protein (red lines = positive correlation; green lines = negative correlation) or protein:protein (blue lines) interactions.
Mentions: To gain an understanding of how the various processes regulated by L/C in wild-type seedlings are connected to each other, and to determine which of these processes are perturbed by the cli186 mutation, a supernode network was created (Figure 2). Supernodes are created by collapsing multiple genes from a multinetwork into a single node, according to their annotation. For example, all genes annotated to the glycolysis/gluconeogenesis pathways are summarized in the network with a single node labeled "glycolysis/gluconeogenesis". The size of the node is proportional to the number of genes annotated to the corresponding node label. Gene edges from the large multinetwork are transferred to the supernode, and are summarized in the final supernode network by a single edge type between supernodes. The connectivity of the nodes are supported by edges that may be metabolic (grey line), protein-DNA (red line = positive correlation; green line = negative correlation) or protein-protein (blue dashed line) interactions or combinations thereof. Hence, this supernode analysis provides a summary of the biological processes that are L/C regulated in wild-type and those that are perturbed by the cli186 mutation and the connections between these processes.

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