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Articulation of three core metabolic processes in Arabidopsis: fatty acid biosynthesis, leucine catabolism and starch metabolism.

Mentzen WI, Peng J, Ransom N, Nikolau BJ, Wurtele ES - BMC Plant Biol. (2008)

Bottom Line: In addition, the co-expression data define a novel hierarchical transcript-level structure associated with catabolism, in which genes performing smaller, more specific tasks appear to be recruited into higher-order modules with a broader catabolic function.Each of these core metabolic pathways is structured as a module of co-expressed transcripts that co-accumulate over a wide range of environmental and genetic perturbations and developmental stages, and represent an expanded set of macromolecules associated with the common task of supporting the functionality of each metabolic pathway.As experimentally demonstrated, co-expression analysis can provide a rich approach towards understanding gene function.

View Article: PubMed Central - HTML - PubMed

Affiliation: 1CRS4 Bioinformatics Laboratory, Loc. Piscinamanna, 09010 Pula, CA, Italy. wiesia@crs4.it

ABSTRACT

Background: Elucidating metabolic network structures and functions in multicellular organisms is an emerging goal of functional genomics. We describe the co-expression network of three core metabolic processes in the genetic model plant Arabidopsis thaliana: fatty acid biosynthesis, starch metabolism and amino acid (leucine) catabolism.

Results: These co-expression networks form modules populated by genes coding for enzymes that represent the reactions generally considered to define each pathway. However, the modules also incorporate a wider set of genes that encode transporters, cofactor biosynthetic enzymes, precursor-producing enzymes, and regulatory molecules. We tested experimentally the hypothesis that one of the genes tightly co-expressed with starch metabolism module, a putative kinase AtPERK10, will have a role in this process. Indeed, knockout lines of AtPERK10 have an altered starch accumulation. In addition, the co-expression data define a novel hierarchical transcript-level structure associated with catabolism, in which genes performing smaller, more specific tasks appear to be recruited into higher-order modules with a broader catabolic function.

Conclusion: Each of these core metabolic pathways is structured as a module of co-expressed transcripts that co-accumulate over a wide range of environmental and genetic perturbations and developmental stages, and represent an expanded set of macromolecules associated with the common task of supporting the functionality of each metabolic pathway. As experimentally demonstrated, co-expression analysis can provide a rich approach towards understanding gene function.

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Metabolic context of Arabidopsis leucine catabolism, starch metabolism and fatty acid biosynthesis pathways (blue rectangles).
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Figure 1: Metabolic context of Arabidopsis leucine catabolism, starch metabolism and fatty acid biosynthesis pathways (blue rectangles).

Mentions: In order to determine how co-expression networks extend across metabolic processes, we selected three core metabolic pathways for analysis: fatty acid biosynthesis, starch metabolism, and mitochondrial leucine catabolism (Fig. 1). These pathways were selected in part because of the authors' extensive knowledge of their structure and biological implications (e.g., [33-39]). Fatty acid biosynthesis is the process by which acetyl-CoA is used to generate acyl moieties that are used as components of cellular membranes, signaling molecules, and molecules that store energy (e.g., seed oils) [40]. Starch is the principal polymeric storage form of glucose, and is stored either transiently in leaves or long-term in seeds [41]. Leucine catabolism provides an alternate source of acetyl-CoA to sustain respiration and metabolic processes in the absence of photosynthesis [42]. We assembled a list of genes with a demonstrated or putative function in these three metabolic pathways; these genes encode not only the enzymes of the "textbook pathway", but also enzymes important for synthesis of cofactors and transporters that are thought to be involved in these processes. Specifically, a set of 126 genes associated with these pathways was identified based upon one of three criteria: 1) genes that were demonstrated by experimental evidence to belong to one of these pathways; 2) genes assigned "putative" functionality in one of these pathways, based on sequence similarity and subcellular localization; or 3) genes encoding transporters and enzymes synthesizing co-factors required for these pathways [see Additional file 1].


Articulation of three core metabolic processes in Arabidopsis: fatty acid biosynthesis, leucine catabolism and starch metabolism.

Mentzen WI, Peng J, Ransom N, Nikolau BJ, Wurtele ES - BMC Plant Biol. (2008)

Metabolic context of Arabidopsis leucine catabolism, starch metabolism and fatty acid biosynthesis pathways (blue rectangles).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2483283&req=5

Figure 1: Metabolic context of Arabidopsis leucine catabolism, starch metabolism and fatty acid biosynthesis pathways (blue rectangles).
Mentions: In order to determine how co-expression networks extend across metabolic processes, we selected three core metabolic pathways for analysis: fatty acid biosynthesis, starch metabolism, and mitochondrial leucine catabolism (Fig. 1). These pathways were selected in part because of the authors' extensive knowledge of their structure and biological implications (e.g., [33-39]). Fatty acid biosynthesis is the process by which acetyl-CoA is used to generate acyl moieties that are used as components of cellular membranes, signaling molecules, and molecules that store energy (e.g., seed oils) [40]. Starch is the principal polymeric storage form of glucose, and is stored either transiently in leaves or long-term in seeds [41]. Leucine catabolism provides an alternate source of acetyl-CoA to sustain respiration and metabolic processes in the absence of photosynthesis [42]. We assembled a list of genes with a demonstrated or putative function in these three metabolic pathways; these genes encode not only the enzymes of the "textbook pathway", but also enzymes important for synthesis of cofactors and transporters that are thought to be involved in these processes. Specifically, a set of 126 genes associated with these pathways was identified based upon one of three criteria: 1) genes that were demonstrated by experimental evidence to belong to one of these pathways; 2) genes assigned "putative" functionality in one of these pathways, based on sequence similarity and subcellular localization; or 3) genes encoding transporters and enzymes synthesizing co-factors required for these pathways [see Additional file 1].

Bottom Line: In addition, the co-expression data define a novel hierarchical transcript-level structure associated with catabolism, in which genes performing smaller, more specific tasks appear to be recruited into higher-order modules with a broader catabolic function.Each of these core metabolic pathways is structured as a module of co-expressed transcripts that co-accumulate over a wide range of environmental and genetic perturbations and developmental stages, and represent an expanded set of macromolecules associated with the common task of supporting the functionality of each metabolic pathway.As experimentally demonstrated, co-expression analysis can provide a rich approach towards understanding gene function.

View Article: PubMed Central - HTML - PubMed

Affiliation: 1CRS4 Bioinformatics Laboratory, Loc. Piscinamanna, 09010 Pula, CA, Italy. wiesia@crs4.it

ABSTRACT

Background: Elucidating metabolic network structures and functions in multicellular organisms is an emerging goal of functional genomics. We describe the co-expression network of three core metabolic processes in the genetic model plant Arabidopsis thaliana: fatty acid biosynthesis, starch metabolism and amino acid (leucine) catabolism.

Results: These co-expression networks form modules populated by genes coding for enzymes that represent the reactions generally considered to define each pathway. However, the modules also incorporate a wider set of genes that encode transporters, cofactor biosynthetic enzymes, precursor-producing enzymes, and regulatory molecules. We tested experimentally the hypothesis that one of the genes tightly co-expressed with starch metabolism module, a putative kinase AtPERK10, will have a role in this process. Indeed, knockout lines of AtPERK10 have an altered starch accumulation. In addition, the co-expression data define a novel hierarchical transcript-level structure associated with catabolism, in which genes performing smaller, more specific tasks appear to be recruited into higher-order modules with a broader catabolic function.

Conclusion: Each of these core metabolic pathways is structured as a module of co-expressed transcripts that co-accumulate over a wide range of environmental and genetic perturbations and developmental stages, and represent an expanded set of macromolecules associated with the common task of supporting the functionality of each metabolic pathway. As experimentally demonstrated, co-expression analysis can provide a rich approach towards understanding gene function.

Show MeSH
Related in: MedlinePlus